Cargando…

Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model

Bordetella (B.) bronchiseptica and Streptococcus (S.) suis are major pathogens in pigs, which are frequently isolated from co-infections in the respiratory tract and contribute to the porcine respiratory disease complex (PRDC). Despite the high impact of co-infections on respiratory diseases of swin...

Descripción completa

Detalles Bibliográficos
Autores principales: Vötsch, Désirée, Willenborg, Maren, Baumgärtner, Wolfgang, Rohde, Manfred, Valentin-Weigand, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7781633/
https://www.ncbi.nlm.nih.gov/pubmed/33372837
http://dx.doi.org/10.1080/21505594.2020.1858604
_version_ 1783631715554557952
author Vötsch, Désirée
Willenborg, Maren
Baumgärtner, Wolfgang
Rohde, Manfred
Valentin-Weigand, Peter
author_facet Vötsch, Désirée
Willenborg, Maren
Baumgärtner, Wolfgang
Rohde, Manfred
Valentin-Weigand, Peter
author_sort Vötsch, Désirée
collection PubMed
description Bordetella (B.) bronchiseptica and Streptococcus (S.) suis are major pathogens in pigs, which are frequently isolated from co-infections in the respiratory tract and contribute to the porcine respiratory disease complex (PRDC). Despite the high impact of co-infections on respiratory diseases of swine (and other hosts), very little is known about pathogen-pathogen-host interactions and the mechanisms of pathogenesis. In the present study, we established a porcine precision-cut lung slice (PCLS) model to analyze the effects of B. bronchiseptica infection on adherence, colonization, and cytotoxic effects of S. suis. We hypothesized that induction of ciliostasis by a clinical isolate of B. bronchiseptica may promote subsequent infection with a virulent S. suis serotype 2 strain. To investigate this theory, we monitored the ciliary activity by light microscopy, measured the release of lactate dehydrogenase, and calculated the number of PCLS-associated bacteria. To study the role of the pore-forming toxin suilysin (SLY) in S. suis-induced cytotoxicity, we included a SLY-negative isogenic mutant and the complemented mutant strain. Furthermore, we analyzed infected PCLS by histopathology, immunofluorescence microscopy, and field emission scanning electron microscopy. Our results showed that pre-infection with B. bronchiseptica promoted adherence, colonization, and, as a consequence of the increased colonization, the cytotoxic effects of S. suis, probably by reduction of the ciliary activity. Moreover, cytotoxicity induced by S. suis is strictly dependent on the presence of SLY. Though the underlying molecular mechanisms remain to be fully clarified, our results clearly support the hypothesis that B. bronchiseptica paves the way for S. suis infection.
format Online
Article
Text
id pubmed-7781633
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Taylor & Francis
record_format MEDLINE/PubMed
spelling pubmed-77816332021-01-13 Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model Vötsch, Désirée Willenborg, Maren Baumgärtner, Wolfgang Rohde, Manfred Valentin-Weigand, Peter Virulence Research Paper Bordetella (B.) bronchiseptica and Streptococcus (S.) suis are major pathogens in pigs, which are frequently isolated from co-infections in the respiratory tract and contribute to the porcine respiratory disease complex (PRDC). Despite the high impact of co-infections on respiratory diseases of swine (and other hosts), very little is known about pathogen-pathogen-host interactions and the mechanisms of pathogenesis. In the present study, we established a porcine precision-cut lung slice (PCLS) model to analyze the effects of B. bronchiseptica infection on adherence, colonization, and cytotoxic effects of S. suis. We hypothesized that induction of ciliostasis by a clinical isolate of B. bronchiseptica may promote subsequent infection with a virulent S. suis serotype 2 strain. To investigate this theory, we monitored the ciliary activity by light microscopy, measured the release of lactate dehydrogenase, and calculated the number of PCLS-associated bacteria. To study the role of the pore-forming toxin suilysin (SLY) in S. suis-induced cytotoxicity, we included a SLY-negative isogenic mutant and the complemented mutant strain. Furthermore, we analyzed infected PCLS by histopathology, immunofluorescence microscopy, and field emission scanning electron microscopy. Our results showed that pre-infection with B. bronchiseptica promoted adherence, colonization, and, as a consequence of the increased colonization, the cytotoxic effects of S. suis, probably by reduction of the ciliary activity. Moreover, cytotoxicity induced by S. suis is strictly dependent on the presence of SLY. Though the underlying molecular mechanisms remain to be fully clarified, our results clearly support the hypothesis that B. bronchiseptica paves the way for S. suis infection. Taylor & Francis 2020-12-29 /pmc/articles/PMC7781633/ /pubmed/33372837 http://dx.doi.org/10.1080/21505594.2020.1858604 Text en © 2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Paper
Vötsch, Désirée
Willenborg, Maren
Baumgärtner, Wolfgang
Rohde, Manfred
Valentin-Weigand, Peter
Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model
title Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model
title_full Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model
title_fullStr Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model
title_full_unstemmed Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model
title_short Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model
title_sort bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of streptococcus suis in a porcine precision-cut lung slice model
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7781633/
https://www.ncbi.nlm.nih.gov/pubmed/33372837
http://dx.doi.org/10.1080/21505594.2020.1858604
work_keys_str_mv AT votschdesiree bordetellabronchisepticapromotesadherencecolonizationandcytotoxicityofstreptococcussuisinaporcineprecisioncutlungslicemodel
AT willenborgmaren bordetellabronchisepticapromotesadherencecolonizationandcytotoxicityofstreptococcussuisinaporcineprecisioncutlungslicemodel
AT baumgartnerwolfgang bordetellabronchisepticapromotesadherencecolonizationandcytotoxicityofstreptococcussuisinaporcineprecisioncutlungslicemodel
AT rohdemanfred bordetellabronchisepticapromotesadherencecolonizationandcytotoxicityofstreptococcussuisinaporcineprecisioncutlungslicemodel
AT valentinweigandpeter bordetellabronchisepticapromotesadherencecolonizationandcytotoxicityofstreptococcussuisinaporcineprecisioncutlungslicemodel